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The Evolutionary History of the Cellophane Bee Genus Colletes

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The Evolutionary History of the Cellophane Bee Genus Colletes Molecular Phylogenetics and Evolution 146 (2020) 106750 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The evolutionary history of the cellophane bee genus Colletes Latreille T (Hymenoptera: Colletidae): Molecular phylogeny, biogeography and implications for a global infrageneric classification ⁎ Rafael R. Ferraria, , Thomas M. Onuferkoa,b, Spencer K. Moncktona, Laurence Packera a Department of Biology, Faculty of Science, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada b The Beaty Centre for Species Discovery, Canadian Museum of Nature, Ottawa, ON K1P 6P4, Canada ARTICLE INFO ABSTRACT Keywords: Colletes Latreille (Hymenoptera: Colletidae) is a diverse genus with 518 valid species distributed in all biogeo- Apoidea graphic realms, except Australasia and Antarctica. Here we provide a comprehensive dated phylogeny for Colletinae Colletes based on Bayesian and maximum likelihood-based analyses of DNA sequence data of six loci: 28S rDNA, Dated phylogeny cytochrome c oxidase subunit 1, elongation factor-1α copy F2, long-wavelength rhodopsin, RNA polymerase II Geodispersal and wingless. In total, our multilocus matrix consists of 4824 aligned base pairs for 143 species, including 112 Historical biogeography Colletes species plus 31 outgroups (one stenotritid and a diverse array of colletids representing all subfamilies). Systematics Overall, analyses of each of the six single-locus datasets resulted in poorly resolved consensus trees with con- flicting phylogenetic signal. However, our analyses of the multilocus matrix provided strong support forthe monophyly of Colletes and show that it can be subdivided into five major clades. The implications of our phy- logenetic results for future attempts at infrageneric classification for the Colletes of the world are discussed. We propose species groups for the Neotropical species of Colletes, the only major biogeographic realm for which no species groups have been proposed to date. Our dating analysis indicated that Colletes diverged from its sister taxon, Hemicotelles Toro and Cabezas, in the early Oligocene and that its extant lineages began diversifying only in the late Oligocene. According to our biogeographic reconstruction, Colletes originated in the Neotropics (most likely within South America) and then spread to the Nearctic very early in its evolutionary history. Geodispersal to the Old World occurred soon after colonization of the Northern Hemisphere. Lastly, the historical biogeo- graphy of Colletes is analyzed in light of available geological and palaeoenvironmental data. 1. Introduction Kuhlmann et al., 2009; Bystriakova et al., 2018; Ascher and Pickering, 2019). A recent analysis of the environmental factors determining the With 518 valid described species, the cellophane bee genus Colletes global distribution of Colletinae demonstrated that their highest species Latreille (Hymenoptera: Colletidae) is the seventh-most diverse of all richness is in the semi-arid regions located at middle latitudes bee genera and second among colletids, after Hylaeus Fabricius (Ascher (Bystriakova et al., 2018). Contrary to Colletes, the other genera of and Pickering, 2019). The actual species richness of Colletes, however, Colletinae—Hemicotelles Toro and Cabezas (2 spp.), Mourecotelles Toro has been estimated to be closer to 700 (Kuhlmann et al., 2009). The and Cabezas (12 spp.) and Xanthocotelles Toro and Cabezas (11 genus has received a significant amount of taxonomic attention over the spp.)—are all confined to South America, most of them to thesub- past decade resulting in a large number of new species (> 70 spp.) tropical and temperate portions of Chile and Argentina (Moure et al., being described (Kuhlmann, 2014a,b; Kuhlmann and Proshchalykin, 2007, 2012). It is important to emphasize that the generic classification 2011, 2013, 2014a, 2015, 2016; Kuhlmann and Pauly, 2013; of Colletinae is controversial, with the number of genera accepted Proshchalykin and Kuhlmann, 2015; Niu et al., 2013a, b, 2014; Ferrari varying from two to six among authors (Toro and Cabezas, 1977, 1978; and Silveira, 2015; Hall et al., 2016; Balboa et al., 2017; Ferrari, 2017, Michener, 1989, 2007; Moure and Urban, 2002; Moure et al., 2007, 2019). Unlike most colletid genera, which have a comparatively re- 2012; Ascher and Pickering, 2019). stricted geographic distribution, Colletes is found in all biogeographic Colletes are typically robust, mid-sized (8–15 mm) bees with rela- realms except Australasia and Antarctica (Michener, 1989, 2007; tively dense pubescence compared to most other colletids (Michener, ⁎ Corresponding author. E-mail address: [email protected] (R.R. Ferrari). https://doi.org/10.1016/j.ympev.2020.106750 Received 20 September 2019; Received in revised form 27 January 2020; Accepted 28 January 2020 Available online 03 February 2020 1055-7903/ © 2020 Elsevier Inc. All rights reserved. R.R. Ferrari, et al. Molecular Phylogenetics and Evolution 146 (2020) 106750 1989, 2007). Morphological synapomorphies supporting the mono- this with the following objectives: (i) to determine the little known phyly of the genus include the form of the subhorizontal surface of the relationships among the NW lineages of Colletes and thus provide a metapostnotum which has a series of longitudinal carinae or sinuous basis for future systematic studies; (ii) to assess the validity of the striae in both sexes (unique within Colletinae), forewings with a sig- currently available subgenera from the OW; and (iii) to reconstruct a moidal second recurrent vein in both sexes (unique among all bees), biogeographic scenario that explains the current distribution of the and T1 subequal in length to T2 in males (unique within Colletinae). genus around the globe in light of geological and palaeoenvironmental Colletes is also monophyletic according to maximum parsimony data. (Kuhlmann et al., 2009) and Bayesian (Almeida and Danforth, 2009; Almeida et al., 2012, 2019) analyses of DNA sequence data; the former 2. Material and methods publication provided the most comprehensive phylogeny for Colletes so far (91 spp.; Kuhlmann et al., 2009) based on two genes (28S rDNA and 2.1. Taxon sampling and specimens studied cytochrome c oxidase subunit 1). With the exception of the subgenus Ptilopoda Friese, which was The subfamilial classification of Colletidae adopted herein follows proposed for an unusual species (C. maculipennis Friese [= C. spilopterus Almeida et al. (2019), in which Paracolletes Smith is a member of Di- Cockerell]) with spotted wings from Central America (Friese, 1921), no phaglossinae, Callomelitta Smith is in its own subfamily, and the other infrageneric classification for Neotropical Colletes has been suggested genera traditionally classified in Paracolletinae (e.g. Michener, 2007, as (Michener, 2007; Kuhlmann et al., 2009). All subgroups proposed Paracolletini) are considered to belong to Neopasiphaeinae. Our taxon within the genus so far—the species groups defined by Noskiewicz, sampling comprises 143 species, 31 of which were sampled as out- Stephen and Kuhlmann as well as all other subgenera (Albocolletes groups and 112 are Colletes (Table S1). Among the outgroups, 22 spe- Warncke, Denticolletes Noskiewicz, Elecolletes Warncke, Nanocolletes cies were chosen to represent the diversity within all colletid sub- Warncke, Pachycolletes Bischoff, Rhinocolletes Cockerell and Simcolletes families based on previous phylogenetic analyses (Magnacca and Warncke)—cover exclusively the Nearctic and/or Old World (OW) Danforth, 2006; Packer, 2008; Almeida and Danforth, 2009; Almeida faunas (Noskiewicz, 1936; Stephen, 1954; Stoeckhert, 1954; Warncke, et al., 2012, 2019). They belong to the following subfamilies: Callo- 1978; Kuhlmann, 2014). All subgenera were subsequently ignored with melittinae (1 sp.), Diphaglossinae (3 spp.), Euryglossinae (3 spp.), Hy- the justification that they had been described for either a single unusual laeinae (4 spp.), Neopasiphaeinae (5 spp.), Scrapterinae (2 spp.) and species (Denticolletes, Ptilopoda and Rhinocolletes) or for artificial groups Xeromelissinae (4 spp.). We also sampled eight species of the other of rather ordinary species (Pachycolletes and Warncke’s subgenera) with genera of Colletinae – Hemicotelles (1 sp.), Mourecotelles (2 spp.) and a restricted geographic distribution in the western Palaearctic Xanthocotelles (5 spp.) – the closest relatives of Colletes (Michener, 1989, (Michener, 1989, 2007). More recently, Kuhlmann et al. (2009) re- 2007; Kuhlmann et al., 2009). The generic classification of Colletinae assessed the status of the available subgenera from the OW and pro- follows Toro and Cabezas (1977, 1978), in which Hemicotelles and posed an updated infrageneric classification for the lineages found Xanthocotelles are recognized as genera (as opposed to subgenera of there, based on their phylogenetic results. Meanwhile, the phylogenetic Mourecotelles; as in Michener, 2007) and Rhynchocolletes Moure is a relationships among the New World (NW) lineages of Colletes remain junior synonym of Colletes (rather than a senior synonym of Mour- poorly understood. The Neotropical Colletes in particular have histori- ecotelles; as in Moure et al., 2007, 2012). Finally, one stenotritid (Ste- cally received much less taxonomic attention compared to those from notritus sp.) was sampled to root the trees given that Stenotridae is the the other biogeographic realms (Michener, 2007: 169). However,
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